Putting the pH into phosphatidic acid signaling

Background

Camouflage patterns that hinder detection and/or recognition by antagonists are widely studied in both human and animal contexts. Patterns of contrasting stripes that purportedly degrade an observer's ability to judge the speed and direction of moving prey ('motion dazzle') are, however, rarely investigated. This is despite motion dazzle having been fundamental to the appearance of warships in both world wars and often postulated as the selective agent leading to repeated patterns on many animals (such as zebra and many fish, snake, and invertebrate species). Such patterns often appear conspicuous, suggesting that protection while moving by motion dazzle might impair camouflage when stationary. However, the relationship between motion dazzle and camouflage is unclear because disruptive camouflage relies on high-contrast markings. In this study, we used a computer game with human subjects detecting and capturing either moving or stationary targets with different patterns, in order to provide the first empirical exploration of the interaction of these two protective coloration mechanisms.

Results

Moving targets with stripes were caught significantly less often and missed more often than targets with camouflage patterns. However, when stationary, targets with camouflage markings were captured less often and caused more false detections than those with striped patterns, which were readily detected.

Conclusions

Our study provides the clearest evidence to date that some patterns inhibit the capture of moving targets, but that camouflage and motion dazzle are not complementary strategies. Therefore, the specific coloration that evolves in animals will depend on how the life history and ontogeny of each species influence the trade-off between the costs and benefits of motion dazzle and camouflage.     

Symmetrical crypsis and asymmetrical signalling in the cuttlefish Sepia officinalis

The salience of bilateral symmetry to humans has led to the suggestion that camouflage may be enhanced in asymmetrical patterns. However, the importance of bilateral symmetry in visual signals (and overall morphology) may constrain the evolution of asymmetrical camouflage, resulting in the bilaterally symmetrical cryptic patterns that we see throughout the animal kingdom. This study investigates the cuttlefish (Sepia officinalis), which can control the degree of symmetry in its coloration. Ten juvenile S. officinalis were filmed in two behavioural contexts (cryptic and threatened) to test the prediction that cryptic patterns will be expressed more asymmetrically than an anti-predator signal known as the 'deimatic display'. Cryptic body patterns, particularly those with a disruptive function, were found to exhibit a high degree of bilateral symmetry. By contrast, the components of the deimatic display were often expressed asymmetrically. These results are contrary to the predicted use of symmetry in defensive coloration, indicating that the role of symmetry in both crypsis and visual signalling is not as straightforward as previously suggested.     

Cuttlefish Sepia officinalis Preferentially Respond to Bottom Rather than Side Stimuli When Not Allowed Adjacent to Tank Walls

Cuttlefish are cephalopods capable of rapid camouflage responses to visual stimuli. However, it is not always clear to what these animals are responding. Previous studies have found cuttlefish to be more responsive to lateral stimuli rather than substrate. However, in previous works, the cuttlefish were allowed to settle next to the lateral stimuli. In this study, we examine whether juvenile cuttlefish (Sepia officinalis) respond more strongly to visual stimuli seen on the sides versus the bottom of an experimental aquarium, specifically when the animals are not allowed to be adjacent to the tank walls. We used the Sub Sea Holodeck, a novel aquarium that employs plasma display screens to create a variety of artificial visual environments without disturbing the animals. Once the cuttlefish were acclimated, we compared the variability of camouflage patterns that were elicited from displaying various stimuli on the bottom versus the sides of the Holodeck. To characterize the camouflage patterns, we classified them in terms of uniform, disruptive, and mottled patterning. The elicited camouflage patterns from different bottom stimuli were more variable than those elicited by different side stimuli, suggesting that S. officinalis responds more strongly to the patterns displayed on the bottom than the sides of the tank. We argue that the cuttlefish pay more attention to the bottom of the Holodeck because it is closer and thus more relevant for camouflage.     

The dual function of barred plumage in birds: camouflage and communication

A commonly held principle in visual ecology is that communication compromises camouflage: while visual signals are often conspicuous, camouflage provides concealment. However, some traits may have evolved for communication and camouflage simultaneously, thereby overcoming this functional compromise. Visual patterns generally provide camouflage, but it was suggested that a particular type of visual pattern – avian barred plumage – could also be a signal of individual quality. Here, we test if the evolution of sexual dimorphism in barred plumage, as well as differences between juvenile and adult plumage, indicate camouflage and/or signalling functions across the class Aves. We found a higher frequency of female- rather than male-biased sexual dimorphism in barred plumage, indicating that camouflage is its most common function. But we also found that, compared to other pigmentation patterns, barred plumage is more frequently biased towards males and its expression more frequently restricted to adulthood, suggesting that barred plumage often evolves or is maintained as a sexual communication signal. This illustrates how visual traits can accommodate the apparently incompatible functions of camouflage and communication, which has implications for our understanding of avian visual ecology and sexual ornamentation.     

The evolution of pattern camouflage strategies in waterfowl and game birds

Visual patterns are common in animals. A broad survey of the literature has revealed that different patterns have distinct functions. Irregular patterns (e.g., stipples) typically function in static camouflage, whereas regular patterns (e.g., stripes) have a dual function in both motion camouflage and communication. Moreover, irregular and regular patterns located on different body regions (“bimodal” patterning) can provide an effective compromise between camouflage and communication and/or enhanced concealment via both static and motion camouflage. Here, we compared the frequency of these three pattern types and traced their evolutionary history using Bayesian comparative modeling in aquatic waterfowl (Anseriformes: 118 spp.), which typically escape predators by flight, and terrestrial game birds (Galliformes: 170 spp.), which mainly use a “sit and hide” strategy to avoid predation. Given these life histories, we predicted that selection would favor regular patterning in Anseriformes and irregular or bimodal patterning in Galliformes and that pattern function complexity should increase over the course of evolution. Regular patterns were predominant in Anseriformes whereas regular and bimodal patterns were most frequent in Galliformes, suggesting that patterns with multiple functions are broadly favored by selection over patterns with a single function in static camouflage. We found that the first patterns to evolve were either regular or bimodal in Anseriformes and either irregular or regular in Galliformes. In both orders, irregular patterns could evolve into regular patterns but not the reverse. Our hypothesis of increasing complexity in pattern camouflage function was supported in Galliformes but not in Anseriformes. These results reveal a trajectory of pattern evolution linked to increasing function complexity in Galliformes although not in Anseriformes, suggesting that both ecology and function complexity can have a profound influence on pattern evolution.     

Plant coloration undermines herbivorous insect camouflage

The main point of our hypothesis "coloration undermines camouflage" is that many color patterns in plants undermine the camouflage of invertebrate herbivores, especially insects, thus exposing them to predation and causing them to avoid plant organs with unsuitable coloration, to the benefit of the plants. This is a common case of "the enemy of my enemy is my friend" and a visual parallel of the chemical signals that plants emit to call wasps when attacked by caterpillars. Moreover, this is also a common natural version of the well-known case of industrial melanism, which illustrates the great importance of plant-based camouflage for herbivorous insects and can serve as an independent test for our hypothesis. We claim that the enormous variations in coloration of leaves, petioles and stems as well as of flowers and fruits undermine the camouflage of invertebrate herbivores, especially insects. We assume that the same principle might operate in certain animal-parasite interactions. Our hypothesis, however, does not contrast or exclude other previous or future explanations of specific types of plant coloration. Traits such as coloration that have more than one type of benefit may be selected for by several agents and evolve more rapidly than ones with a single type of advantage.     

Camouflage in predators

Camouflage – adaptations that prevent detection and/or recognition – is a key example of evolution by natural selection, making it a primary focus in evolutionary ecology and animal behaviour. Most work has focused on camouflage as an anti‐predator adaptation. However, predators also display specific colours, patterns and behaviours that reduce visual detection or recognition to facilitate predation. To date, very little attention has been given to predatory camouflage strategies. Although many of the same principles of camouflage studied in prey translate to predators, differences between the two groups (in motility, relative size, and control over the time and place of predation attempts) may alter selection pressures for certain visual and behavioural traits. This makes many predatory camouflage techniques unique and rarely documented. Recently, new technologies have emerged that provide a greater opportunity to carry out research on natural predator–prey interactions. Here we review work on the camouflage strategies used by pursuit and ambush predators to evade detection and recognition by prey, as well as looking at how work on prey camouflage can be applied to predators in order to understand how and why specific predatory camouflage strategies may have evolved. We highlight that a shift is needed in camouflage research focus, as this field has comparatively neglected camouflage in predators, and offer suggestions for future work that would help to improve our understanding of camouflage.     

The colouration of the venomous coral snakes (family Elapidae) and their mimics (families Aniliidae and Golubridae)

The bright coloured, highly venomous coral snakes, Leptomicrurus, Micrurus and Micruroides (family Elapidae) and a series of harmless or mildly toxic mimics form an important component of the snake fauna of the Americas. Coral snake patterns are defined as any dorsal pattern found in any species of venomous coral snake and/or any dorsal pattern containing a substantial amount of red, pink or orange distributed so as to resemble that of some species of venomous coral snake. The components of coral snake colouration are described and four principal dorsal patterns are recognized: unicolour, bicolour, tricolour and quadricolour. The tricolour patterns may be further clustered based on the number of black bands or rings separating the red ones as: monads, dyads, triads, tetrads or pentads. A detailed classification of all coral snake colour patterns is presented and each pattern is illustrated. The taxonomic distribution of these patterns is surveyed for mimics and the 56 species of highly venomous coral snakes. Among the latter, the most frequent encountered patterns are tricolour monads, tricolour triads and bicolour rings, in that order. No venomous coral snakes have a tricolour dyad, tricolour tetrad or quadricolour pattern. As many as 115 species of harmless or mildly toxic species, c. 18% of all American snakes, are regarded as coral snake mimics. The colouration and behavioural traits of venomous coral snakes combine to form a significant antipredator defence of an aposematic type. The mimics in turn receive protection from predators that innately or through learning avoid coral snake colour patterns. The precise resemblances in colouration between sympatric non-coral snakes and venomous coral snakes and the concordant geographic variation between the two strongly support this view. Batesian mimicry with the highly venomous coral snakes as the models and the other forms as the mimics is the favoured explanation for this situation. It is further concluded that a number of species in the genera Elaphe, Farancia, Nerodia and Thamnophis, although having red in their colouration, should not be included in the coral snake mimic guild.     

Camouflage patterns in Nautilus, and their implications for cephalopod paleobiology

Cowen, R., Gertman, R. & Wiggett, Gail: Camouflage patterns in Nautilus , and their implications for cephalopod paleobiology.
Formal analysis of the pigment patterns of adult Nautilus shows that they are perfectly camouflaged for life in open water. But because of their accretionary growth pattern, juveniles are not fully camouflaged for open water: this supports previous suggestions that young Nautilus are benthonic. The principles of camouflage are used to re-assess some facets of cephalopod paleobiology. The life orientation of some early cyrtocones is re-interpreted. 'Ornament' on ammonoids is seen as camouflage structure, and we infer photic-nektonic, photic-benthonic, and aphotic habitats for three major morphological groups of ammonites. Sexual dimorphism in ammonites was probably accompanied by sexual separation in habitat, except for a short (annual) mating season. This is not inconsistent with modern cephalopod biology.     

Cuttlefish dynamic camouflage: responses to substrate choice and integration of multiple visual cues

Prey camouflage is an evolutionary response to predation pressure. Cephalopods have extensive camouflage capabilities and studying them can offer insight into effective camouflage design. Here, we examine whether cuttlefish, Sepia officinalis, show substrate or camouflage pattern preferences. In the first two experiments, cuttlefish were presented with a choice between different artificial substrates or between different natural substrates. First, the ability of cuttlefish to show substrate preference on artificial and natural substrates was established. Next, cuttlefish were offered substrates known to evoke three main camouflage body pattern types these animals show: Uniform or Mottle (function by background matching); or Disruptive. In a third experiment, cuttlefish were presented with conflicting visual cues on their left and right sides to assess their camouflage response. Given a choice between substrates they might encounter in nature, we found no strong substrate preference except when cuttlefish could bury themselves. Additionally, cuttlefish responded to conflicting visual cues with mixed body patterns in both the substrate preference and split substrate experiments. These results suggest that differences in energy costs for different camouflage body patterns may be minor and that pattern mixing and symmetry may play important roles in camouflage.     

Are Stripes Beneficial? Dazzle Camouflage Influences Perceived Speed and Hit Rates

In the animal kingdom, camouflage refers to patterns that help potential prey avoid detection. Mostly camouflage is thought of as helping prey blend in with their background. In contrast, disruptive or dazzle patterns protect moving targets and have been suggested as an evolutionary force in shaping the dorsal patterns of animals. Dazzle patterns, such as stripes and zigzags, are thought to reduce the probability with which moving prey will be captured by impairing predators'' perception of speed. We investigated how different patterns of stripes (longitudinal—i.e., parallel to movement direction–and vertical–i.e., perpendicular to movement direction) affect the probability with which humans can hit moving objects and if differences in hitting probability are caused by a misperception of speed. A first experiment showed that longitudinally striped objects were hit more often than unicolored objects. However, vertically striped objects did not differ from unicolored objects. A second study examining the link between perceived speed and hitting probability showed that longitudinally and vertically striped objects were both perceived as moving faster and were hit more often than unicolored objects. In sum, our results provide evidence that striped patterns disrupt the perception of speed, which in turn influences how often objects are hit. However, the magnitude and the direction of the effects depend on additional factors such as speed and the task setup.     

Becoming a Sign: The Mimic’s Activity in Biological Mimicry

From a semiotic perspective biological mimicry can be described as a tripartite system with a double structure that consists of ecological relations between species and semiotic relations of sign. In this article the focus is on the mimic who is the individual benefiting from its resemblance to the cues or signals of other species or to the environment. In establishing the mimetic resemblance the question of mimic’s activity becomes crucial, and the activity can range from the fixed bodily patterns to fully dynamic behavioural displays. The mimic’s activity can be targeted at two other participants of the mimicry system—either at the model or at the receiver. The first possibility is quite common in camouflage and there are several possibilities for mimic’s activity to occur: selecting a resting place or habitat based on conformity with the environment, changing body coloration to correspond to the surrounding environment, covering oneself with particles of the soil. In its activity aimed at the model, the mimic develops a strong semiotic connection with its specific perceptual environment or part of it and obtains a representational character. In the second possibility the activity of a mimetic organism is aimed at the receiver who is confused by the resemblance, and between the two participants an active communicative interaction is established. Such type of mimicry can be exemplified by abstract threat displays found in various groups of animals, for instance a toad’s upright posture as a response to the presence of a snake. From the semiotic viewpoint it can be interpreted as the motive of fear in the predator’s Umwelt being entered into the mimic’s subjective world and manifested in its behaviour. The mimetic organism ends up in an ambiguous position, where it needs to pretend to be something other than it is. In the final part of the article it is argued that the mimetic sign is basically a false designator as the mimic’s activity to become a sign is aimed at a specific type of signs. Rather than signifying belonging to its own species or group, a mimetic sign indicates that its carrier belongs to the type of some other species. The tension between the form and behaviour of mimetic organisms arises from the discrepancy between the type of organism that it essentially is and the type of organism that the mimetic sign it carries imposes on it.     

Enhancement of chromatic contrast increases predation risk for striped butterflies

Many prey species have evolved defensive colour patterns to avoid attacks. One type of camouflage, disruptive coloration, relies on contrasting patterns that hinder predators' ability to recognize an object. While high contrasts are used to facilitate detection in many visual communication systems, they are thought to provide misleading information about prey appearance in disruptive patterns. A fundamental tenet in disruptive coloration theory is the principle of 'maximum disruptive contrast', i.e. disruptive patterns are more effective when higher contrasts are involved. We tested this principle in highly contrasting stripes that have often been described as disruptive patterns. Varying the strength of chromatic contrast between stripes and adjacent pattern elements in artificial butterflies, we found a strong negative correlation between survival probability and chromatic contrast strength. We conclude that too high a contrast leads to increased conspicuousness rather than to effective camouflage. However, artificial butterflies that sported contrasts similar to those of the model species Limenitis camilla survived equally well as background-matching butterflies without these stripes. Contrasting stripes do thus not necessarily increase predation rates. This result may provide new insights into the design and characteristics of a range of colour patterns such as sexual, mimetic and aposematic signals.     

Elevational gradients of diversity for lizards and snakes in the Hengduan Mountains,China

Comparing elevational gradients across a wide spectrum of climatic zones offers an ideal system for testing hypotheses explaining the altitudinal gradients of biodiversity. We document elevational patterns of lizard and snake species richness, and explore how land area and climatic factors may affect species distributions of lizards and snakes. Our synthesis found 42 lizard species and 94 snake species known from the Hengduan Mountains. The lizards are distributed between 500 and 3500 m, and the snakes are distributed between 500 and 4320 m. The relationship between species richness and elevation for lizards and snakes is unimodal. Land area explains a significant amount of the variation in lizard and snake species richness. The cluster analysis reveals pronounced distinct assemblages for lizards and snakes to better reflect the vertical profiles of climate in the mountains. Climatic variables are strongly associated with lizard and snake richness along the elevational gradient. The data strongly implicate water availability as a key constraint on lizard species richness, and annual potential evapotranspiration is the best predictor of snake species richness along the elevational gradient in the Hengduan Mountains.     

Cognition and the evolution of camouflage

Camouflage is one of the most widespread forms of anti-predator defence and prevents prey individuals from being detected or correctly recognized by would-be predators. Over the past decade, there has been a resurgence of interest in both the evolution of prey camouflage patterns, and in understanding animal cognition in a more ecological context. However, these fields rarely collide, and the role of cognition in the evolution of camouflage is poorly understood. Here, we review what we currently know about the role of both predator and prey cognition in the evolution of prey camouflage, outline why cognition may be an important selective pressure driving the evolution of camouflage and consider how studying the cognitive processes of animals may prove to be a useful tool to study the evolution of camouflage, and vice versa. In doing so, we highlight that we still have a lot to learn about the role of cognition in the evolution of camouflage and identify a number of avenues for future research.     

Cuttlefish camouflage: context-dependent body pattern use during motion

It is virtually impossible to camouflage a moving target against a non-uniform background, but strategies have been proposed to reduce detection and targeting of movement. Best known is the idea that high contrast markings produce ‘motion dazzle’, which impairs judgement of speed and trajectory. The ability of the cuttlefish Sepia officinalis to change its visual appearance allows us to compare the animal''s choice of patterns during movement to the predictions of models of motion camouflage. We compare cuttlefish body patterns used during movement with those expressed when static on two background types; one of which promotes low-contrast mottle patterns and the other promotes high-contrast disruptive patterns. We find that the body pattern used during motion is context-specific and that high-contrast body pattern components are significantly reduced during movement. Thus, in our experimental conditions, cuttlefish do not use high contrast motion dazzle. It may be that, in addition to being inherently conspicuous during movement, moving high-contrast patterns will attract attention because moving particles in coastal waters tend to be of small size and of low relative contrast.     

Perception of visual texture and the expression of disruptive camouflage by the cuttlefish, Sepia officinalis

Juvenile cuttlefish (Sepia officinalis) camouflage themselves by changing their body pattern according to the background. This behaviour can be used to investigate visual perception in these molluscs and may also give insight into camouflage design. Edge detection is an important aspect of vision, and here we compare the body patterns that cuttlefish produced in response to checkerboard backgrounds with responses to backgrounds that have the same spatial frequency power spectrum as the checkerboards, but randomized spatial phase. For humans, phase randomization removes visual edges. To describe the cuttlefish body patterns, we scored the level of expression of 20 separate pattern 'components', and then derived principal components (PCs) from these scores. After varimax rotation, the first component (PC1) corresponded closely to the so-called disruptive body pattern, and the second (PC2) to the mottle pattern. PC1 was predominantly expressed on checkerboards, and PC2 on phase-randomized backgrounds. Thus, cuttlefish probably have edge detectors that control the expression of disruptive pattern. Although the experiments used unnatural backgrounds, it seems probable that cuttlefish display disruptive camouflage when there are edges in the visual background caused by discrete objects such as pebbles. We discuss the implications of these findings for our understanding of disruptive camouflage.     

Perception of edges and visual texture in the camouflage of the common cuttlefish, Sepia officinalis

The cuttlefish, Sepia officinalis, provides a fascinating opportunity to investigate the mechanisms of camouflage as it rapidly changes its body patterns in response to the visual environment. We investigated how edge information determines camouflage responses through the use of spatially high-pass filtered 'objects' and of isolated edges. We then investigated how the body pattern responds to objects defined by texture (second-order information) compared with those defined by luminance. We found that (i) edge information alone is sufficient to elicit the body pattern known as Disruptive, which is the camouflage response given when a whole object is present, and furthermore, isolated edges cause the same response; and (ii) cuttlefish can distinguish and respond to objects of the same mean luminance as the background. These observations emphasize the importance of discrete objects (bounded by edges) in the cuttlefish's choice of camouflage, and more generally imply that figure-ground segregation by cuttlefish is similar to that in vertebrates, as might be predicted by their need to produce effective camouflage against vertebrate predators.     

Correlations between Ontogenetic Change in Color Pattern and Antipredator Behavior in the Racer, Coluber constrictor

Differences in snake color pattern have been demonstrated to affect behaviors involved in antipredator defense. Snakes with blotched or banded color patterns are concealed when not moving, and tend to rely on concealment and aggression for defense. In contrast, snakes with uniform or striped color patterns are easily seen when stationary, but their speed and direction are difficult to track when moving. They tend to rely on flight for protection. Some snake taxa exhibit ontogenetic change in color pattern, but the behavioral consequences of this change have not been investigated. I present results of a behavioral study in the racer, Coluber constrictor, which has a blotched juvenile color pattern but is uniformly colored as an adult. Hatchling racers were significantly more likely than adults to show aggressive behavior when confronted with a model predator, whereas adults were more likely to flee. This supports the hypothesis that changes in behavior and color pattern are correlated in this species to provide effective antipredator defense at different stages of life history. I also examined sprint speed, which may be an important factor in antipredator defense. Juvenile and adult racers showed a similar relationship between length and speed, a pattern also seen in other species that lack color change. This result suggests that sprint speed is not a causal factor in the evolution of ontogenetic color change.